Why infectious disease research needs community ecology

Science

Volumn 349, Issue 6252, 2015, Pages

  Johnson, Pieter T J ^a   De Roode, Jacobus C ^b   Fenton, Andy ^c  

^a UNIVERSITY OF COLORADO   (United States)

^b EMORY UNIVERSITY   (United States)

^c UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COMMUNITY ECOLOGY; DISEASE CONTROL; DISEASE VECTOR; HETEROGENEITY; INFECTIOUS DISEASE; PATHOLOGY;

BABESIA MICROTI; BARTONELLA; BIODIVERSITY; BODY SIZE; BOVINE TUBERCULOSIS; COMMUNITY ECOLOGY; COMMUNITY STRUCTURE; CONTROL STRATEGY; DISEASE CARRIER; DOMESTIC ANIMAL; EPIDEMIC; GEOGRAPHY; HABITAT; HOME RANGE; HOST PARASITE INTERACTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; INFECTION; INFECTION CONTROL; INFECTION RISK; INVASIVE SPECIES; LIVESTOCK; LONGEVITY; LYME DISEASE; MALARIA; MEDICAL RESEARCH; MICROBIAL COMMUNITY; MICROTUS AGRESTIS; MIXED INFECTION; NONHUMAN; PARASITE TRANSMISSION; PHYLOGENY; POPULATION GENETICS; PRIORITY JOURNAL; REVIEW; SEVERE ACUTE RESPIRATORY SYNDROME; SPECIES; SYMBIONT; TICK BORNE ENCEPHALITIS VIRUS; TUBERCULOSIS; TYPHOID FEVER; VACCINATION; VIRULENCE; ANIMAL; BIOTA; COMMUNICABLE DISEASES; PROCEDURES; SYMBIOSIS;

EBOLA VIRUS;

ANIMALS; BIOTA; COMMUNICABLE DISEASE CONTROL; COMMUNICABLE DISEASES; HOST-PARASITE INTERACTIONS; HUMANS; SYMBIOSIS;

EID: 84941370230     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.1259504     Document Type: Review

References (105)

1. B. Jasny, L. Roberts, M. Enserink, O. Smith, What works [introduction to Global Health special issue]. Science 345, 1256-1257 (2014). doi:10.1126/science.345.6202.1256; pmid: 25214599.
2. J. Sepúlveda, C. Murray, The state of global health in 2014. Science 345, 1275-1278 (2014). pmid: 25214611.
3. World Health Organization, The Top 10 Causes of Death (2014); www.who.int/mediacentre/factsheets/fs310/en.
4. M. C. Fisher et al., Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186-194 (2012). doi:10.1038/nature10947; pmid: 22498624.
5. B. V. Purse et al., Climate change and the recent emergence of bluetongue in Europe. Nat. Rev. Microbiol. 3, 171-181 (2005). doi:10.1038/nrmicro1090; pmid: 15685226.
6. K. F. Smith et al., Global rise in human infectious disease outbreaks. J. R. Soc. Interface 11, 20140950 (2014). doi:10.1098/rsif.2014.0950; pmid: 25401184.
7. K. E. Jones et al., Global trends in emerging infectious diseases. Nature 451, 990-993 (2008). doi:10.1038/nature06536; pmid: 18288193.
8. J. O. Lloyd-Smith et al., Epidemic dynamics at the human-animal interface. Science 326, 1362-1367 (2009). doi:10.1126/science.1177345; pmid: 19965751.
9. A. M. Messenger, A. N. Barnes, G. C. Gray, Reverse zoonotic disease transmission (zooanthroponosis): A systematic review of seldom-documented human biological threats to animals. PLOS ONE 9, e89055 (2014). doi:10.1371/journal.pone.0089055; pmid: 24586500.
10. J. W. Rudge et al., Identifying host species driving transmission of schistosomiasis japonica, a multihost parasite system, in China. Proc. Natl. Acad. Sci. U.S.A. 110, 11457-11462 (2013). doi:10.1073/pnas.1221509110; pmid: 23798418.
11. J. E. Rabinovich et al., Ecological patterns of blood-feeding by kissing-bugs (Hemiptera: Reduviidae: Triatominae). Mem. Inst. Oswaldo Cruz 106, 479-494 (2011). doi:10.1590/S0074-02762011000400016 pmid: 21739038.
12. S. Alizon, J. C. de Roode, Y. Michalakis, Multiple infections and the evolution of virulence. Ecol. Lett. 16, 556-567 (2013). doi:10.1111/ele.12076; pmid: 23347009.
13. A. B. Pedersen, A. Fenton, Emphasizing the ecology in parasite community ecology. Trends Ecol. Evol. 22, 133-139 (2007). doi:10.1016/j.tree.2006.11.005; pmid: 17137676.
14. S. Telfer et al., Species interactions in a parasite community drive infection risk in a wildlife population. Science 330, 243-246 (2010). doi:10.1126/science.1190333; pmid: 20929776.
15. C. K. Kwan, J. D. Ernst, HIV and tuberculosis: A deadly human syndemic. Clin. Microbiol. Rev. 24, 351-376 (2011). doi:10.1128/CMR.00042-10 pmid: 21482729.
16. P. Druilhe, A. Tall, C. Sokhna, Worms can worsen malaria: Towards a new means to roll back malaria? Trends Parasitol. 21, 359-362 (2005). doi:10.1016/j.pt.2005.06.011; pmid: 15967721.
17. A. K. Gibson et al., Polyparasitism is associated with increased disease severity in Toxoplasma gondii-infected marine sentinel species. PLOS Negl. Trop. Dis. 5, e1142 (2011). doi:10.1371/journal.pntd.0001142; pmid: 21629726.
18. J. D. Voss, D. K. Mills, J. L. Myers, E. R. Remily, L. L. Richardson, Black band disease microbial community variation on corals in three regions of the wider Caribbean. Microb. Ecol. 54, 730-739 (2007). doi:10.1007/s00248-007-9234-1; pmid: 17393054.
19. H. Susi, B. Barrès, P. F. Vale, A. L. Laine, Co-infection alters population dynamics of infectious disease. Nat. Commun. 6, 5975 (2015). doi:10.1038/ncomms6975; pmid: 25569306.
20. D. F. Doak et al., Understanding and predicting ecological dynamics: Are major surprises inevitable? Ecology 89, 952-961 (2008). doi:10.1890/07-0965.1 pmid: 18481520.
21. J. A. Al-Tawfiq, Z. A. Memish, Middle East respiratory syndrome coronavirus: Transmission and phylogenetic evolution. Trends Microbiol. 22, 573-579 (2014). pmid: 25178651.
22. P. J. Hudson, S. E. Perkins, I. M. Cattadori, in Infectious Disease Ecology: Effects of Ecosystems on Disease and of Disease on Ecosystems, R. S. Ostfeld, F. Keesing, V. T. Eviner, Eds. (Princeton Univ. Press, Princeton, NJ, 2008), pp. 347-367.
23. R. Woodroffe et al., Culling and cattle controls influence tuberculosis risk for badgers. Proc. Natl. Acad. Sci. U.S.A. 103, 14713-14717 (2006). doi:10.1073/pnas.0606251103; pmid: 17015843.
24. J. R. Mihaljevic, Linking metacommunity theory and symbiont evolutionary ecology. Trends Ecol. Evol. 27, 323-329 (2012). doi:10.1016/j.tree.2012.01.011; pmid: 22341499.
25. E. C. Rynkiewicz, A. B. Pedersen, A. Fenton, An ecosystem approach to understanding and managing within-host parasite community dynamics. Trends Parasitol. 31, 212-221 (2015). doi:10.1016/j.pt.2015.02.005; pmid: 25814004.
26. E. W. Seabloom et al., The community ecology of pathogens: Coinfection, coexistence and community composition. Ecol. Lett. 18, 401-415 (2015). doi:10.1111/ele.12418; pmid: 25728488.
27. R. D. Holt, A. Dobson, in Disease Ecology: Community Structure and Pathogen Dynamics, S. K. Collinge, C. Ray, Eds. (Oxford Univ. Press, Oxford, 2006), pp. 6-27.
28. M. Vellend, Conceptual synthesis in community ecology. Q. Rev. Biol. 85, 183-206 (2010). doi:10.1086/652373; pmid: 20565040.
29. P. B. Adler, J. Hille Ris Lambers, J. M. Levine, A niche for neutrality. Ecol. Lett. 10, 95-104 (2007).doi:10.1111/j.1461-0248.2006.00996.x; pmid: 17257097.
30. J. M. Chase, Drought mediates the importance of stochastic community assembly. Proc. Natl. Acad. Sci. U.S.A. 104, 17430-17434 (2007). doi:10.1073/pnas.0704350104; pmid: 17942690.
31. A. F. Read, L. H. Taylor, The ecology of genetically diverse infections. Science 292, 1099-1102 (2001). doi:10.1126/science.1059410; pmid: 11352063.
32. M. A. Leibold et al., The metacommunity concept: A framework for multi-scale community ecology. Ecol. Lett. 7, 601-613 (2004). doi: 10.1111/j.1461-0248.2004.00608.x.
33. S. J. Presley, C. L. Higgins, M. R. Willig, A comprehensive framework for the evaluation of metacommunity structure. Oikos 119, 908-917 (2010). doi: 10.1111/j.1600-0706.2010.18544.x.
34. G. Suzán et al., Metacommunity and phylogenetic structure determine wildlife and zoonotic infectious disease patterns in time and space. Ecol. Evol. 5, 865-873 (2015). doi:10.1002/ece3.1404; pmid: 25750713.
35. T. Dallas, S. J. Presley, Relative importance of host environment, transmission potential and host phylogeny to the structure of parasite metacommunities. Oikos 123, 866-874 (2014). doi: 10.1111/oik.00707.
36. I. M. Parker et al., Phylogenetic structure and host abundance drive disease pressure in communities. Nature 520, 542-544 (2015). doi:10.1038/nature14372; pmid: 25903634.
37. P. T. J. Johnson, D. L. Preston, J. T. Hoverman, B. E. LaFonte, Host and parasite diversity jointly control disease risk in complex communities. Proc. Natl. Acad. Sci. U.S.A. 110, 16916-16921 (2013). doi:10.1073/pnas.1310557110; pmid: 24082092.
38. R. Poulin, Network analysis shining light on parasite ecology and diversity. Trends Parasitol. 26, 492-498 (2010). doi:10.1016/j.pt.2010.05.008; pmid: 20561821.
39. E. C. Griffiths, A. B. Pedersen, A. Fenton, O. L. Petchey, Analysis of a summary network of co-infection in humans reveals that parasites interact most via shared resources. Proc. R. Soc. B 281, 20132286 (2014). doi:10.1098/rspb.2013.2286; pmid: 24619434.
40. S. Davis, B. Abbasi, S. Shah, S. Telfer, M. Begon, Spatial analyses of wildlife contact networks. J. R. Soc. Interface 12, 20141004 (2014). doi:10.1098/rsif.2014.1004; pmid: 25411407.
41. D. M. Tompkins, A. M. Dunn, M. J. Smith, S. Telfer, Wildlife diseases: From individuals to ecosystems. J. Anim. Ecol. 80, 19-38 (2011). doi:10.1111/j.1365-2656.2010.01742.x; pmid: 20735792.
42. A. R. Cirtwill, D. B. Stouffer, Concomitant predation on parasites is highly variable but constrains the ways in which parasites contribute to food web structure. J. Anim. Ecol. 84, 734-744 (2015). doi:10.1111/1365-2656.12323; pmid: 25418425.
43. T. Poisot, E. Canard, D. Mouillot, N. Mouquet, D. Gravel, The dissimilarity of species interaction networks. Ecol. Lett. 15, 1353-1361 (2012). doi:10.1111/ele.12002; pmid: 22994257.
44. B. J. McGill, B. J. Enquist, E. Weiher, M. Westoby, Rebuilding community ecology from functional traits. Trends Ecol. Evol. 21, 178-185 (2006). doi:10.1016/j.tree.2006.02.002 pmid: 16701083.
45. C. T. Webb, J. A. Hoeting, G. M. Ames, M. I. Pyne, N. LeRoy Poff, A structured and dynamic framework to advance traits-based theory and prediction in ecology. Ecol. Lett. 13, 267-283 (2010). doi:10.1111/j.1461-0248.2010.01444.x; pmid: 20455917.
46. E. Weiher et al., Advances, challenges and a developing synthesis of ecological community assembly theory. Philos. Trans. R. Soc. B 366, 2403-2413 (2011). doi:10.1098/rstb.2011.0056; pmid: 21768155.
47. B. A. Han, J. P. Schmidt, S. E. Bowden, J. M. Drake, Rodent reservoirs of future zoonotic diseases. Proc. Natl. Acad. Sci. U.S.A. 112, 7039-7044 (2015). doi:10.1073/pnas.1501598112; pmid: 26038558.
48. S. H. Paull et al., From superspreaders to disease hotspots: Linking transmission across hosts and space. Front. Ecol. Environ. 10, 75-82 (2012). doi:10.1890/110111; pmid: 23482675.
49. D. G. Streicker, A. Fenton, A. B. Pedersen, Differential sources of host species heterogeneity influence the transmission and control of multihost parasites. Ecol. Lett. 16, 975-984 (2013). doi:10.1111/ele.12122; pmid: 23714379.
50. J. O. Lloyd-Smith, S. J. Schreiber, P. E. Kopp, W. M. Getz, Superspreading and the effect of individual variation on disease emergence. Nature 438, 355-359 (2005). doi:10.1038/nature04153; pmid: 16292310.
51. Z. Shen et al., Superspreading SARS events, Beijing, 2003. Emerg. Infect. Dis. 10, 256-260 (2004). doi:10.3201/eid1002.030732; pmid: 15030693.
52. A. L. Graham et al., Fitness correlates of heritable variation in antibody responsiveness in a wild mammal. Science 330, 662-665 (2010). doi:10.1126/science.1194878; pmid: 21030656.
53. S. E. Perkins, I. M. Cattadori, V. Tagliapietra, A. P. Rizzoli, P. J. Hudson, Empirical evidence for key hosts in persistence of a tick-borne disease. Int. J. Parasitol. 33, 909-917 (2003). doi:10.1016/S0020-7519(03)00128-0; pmid: 12906875.
54. W. E. Stutz, O. L. Lau, D. I. Bolnick, Contrasting patterns of phenotype-dependent parasitism within and among populations of threespine stickleback. Am. Nat. 183, 810-825 (2014). doi:10.1086/676005; pmid: 24823824.
55. D. G. Streicker, A. Fenton, A. B. Pedersen, Differential sources of host species heterogeneity influence the transmission and control of multihost parasites. Ecol. Lett. 16, 975-984 (2013). doi:10.1111/ele.12122 pmid: 23714379.
56. J. M. Calabrese, J. L. Brunner, R. S. Ostfeld, Partitioning the aggregation of parasites on hosts into intrinsic and extrinsic components via an extended Poisson-gamma mixture model. PLOS ONE 6, e29215 (2011). doi:10.1371/journal.pone.0029215; pmid: 22216216.
57. P. Chesson, Scale transition theory: Its aims, motivations and predictions. Ecol. Complex. 10, 52-68 (2012). doi: 10.1016/j.ecocom.2011.11.002.
58. A. Fenton, S. E. Perkins, Applying predator-prey theory to modelling immune-mediated, within-host interspecific parasite interactions. Parasitology 137, 1027-1038 (2010). doi:10.1017/S0031182009991788; pmid: 20152061.
59. R. M. Anderson, R. M. May, Regulation and stability of hostparasite population interactions. I. Regulatory processes. J. Anim. Ecol. 47, 219-247 (1978). doi: 10.2307/3933.
60. R. M. Anderson, R. M. May, The population dynamics of microparasites and their invertebrate hosts. Philos. Trans. R. Soc. London Ser. B 291, 451-524 (1981). doi: 10.1098/rstb.1981.0005.
61. R. R. Dunn, T. J. Davies, N. C. Harris, M. C. Gavin, Global drivers of human pathogen richness and prevalence. Proc. R. Soc. B 277, 2587-2595 (2010). doi:10.1098/rspb.2010.0340; pmid: 20392728.
62. S. C. L. Knowles et al., Stability of within-host-parasite communities in a wild mammal system. Proc. R. Soc. B 280, 20130598 (2013). doi:10.1098/rspb.2013.0598; pmid: 23677343.
63. V. O. Ezenwa, A. E. Jolles, Opposite effects of anthelmintic treatment on microbial infection at individual versus population scales. Science 347, 175-177 (2015). doi:10.1126/science.1261714; pmid: 25574023.
64. A. Fenton, Dances with worms: The ecological and evolutionary impacts of deworming on coinfecting pathogens. Parasitology 140, 1119-1132 (2013). doi:10.1017/S0031182013000590; pmid: 23714427.
65. R. S. Ostfeld, F. Keesing, Effects of host diversity on infectious disease. Annu. Rev. Ecol. Evol. Syst. 43, 157-182 (2012). doi: 10.1146/annurev-ecolsys-102710-145022.
66. P. T. J. Johnson, R. S. Ostfeld, F. Keesing, Frontiers in research on biodiversity and disease. Ecol. Lett. (2015). doi: 10.1111/ele.12479.
67. D. W. Schindler, Replication versus realism: The need for ecosystem-scale experiments. Ecosystems 1, 323-334 (1998). doi: 10.1007/s100219900026.
68. A. B. Pedersen, A. Fenton, The role of antiparasite treatment experiments in assessing the impact of parasites on wildlife. Trends Parasitol. 31, 200-211 (2015). doi:10.1016/j.pt.2015.02.004; pmid: 25778845.
69. D. A. Grear, S. E. Perkins, P. J. Hudson, Does elevated testosterone result in increased exposure and transmission of parasites? Ecol. Lett. 12, 528-537 (2009). doi:10.1111/j.1461-0248.2009.01306.x; pmid: 19392718.
70. A. B. Pedersen, T. J. Greives, The interaction of parasites and resources cause crashes in a wild mouse population. J. Anim. Ecol. 77, 370-377 (2008). doi:10.1111/j.1365-2656.2007.01321.x; pmid: 18028357.
71. P. T. J. Johnson, D. L. Preston, J. T. Hoverman, K. L. D. Richgels, Biodiversity decreases disease through predictable changes in host community competence. Nature 494, 230-233 (2013). doi:10.1038/nature11883; pmid: 23407539.
72. G. Suzán et al., Experimental evidence for reduced rodent diversity causing increased hantavirus prevalence. PLOS ONE 4, e5461 (2009). pmid: 19421313.
73. K. E. Langwig et al., Context-dependent conservation responses to emerging wildlife diseases. Front. Ecol. Environ. 13, 195-202 (2015). doi: 10.1890/140241.
74. K. L. S. Drury, J. D. Rothlisberger, Offense and defense in landscape-level invasion control. Oikos 117, 182-190 (2008). doi: 10.1111/j.2007.0030-1299.16081.x.
75. F. Keesing et al., Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468, 647-652 (2010). doi:10.1038/nature09575; pmid: 21124449.
76. A. O. Franco, M. G. M. Gomes, M. Rowland, P. G. Coleman, C. R. Davies, Controlling malaria using livestock-based interventions: A one health approach. PLOS ONE 9, e101699 (2014). doi:10.1371/journal.pone.0101699; pmid: 25050703.
77. B. Kaabi, S. B. Ahmed, Assessing the effect of zooprophylaxis on zoonotic cutaneous leishmaniasis transmission: A system dynamics approach. Biosystems 114, 253-260 (2013). doi:10.1016/j.biosystems.2013.10.003; pmid: 24157699.
78. Y. Zhu et al., Genetic diversity and disease control in rice. Nature 406, 718-722 (2000). doi:10.1038/35021046; pmid: 10963595.
79. D. J. Civitello et al., Biodiversity inhibits parasites: Broad evidence for the dilution effect. Proc. Natl. Acad. Sci. U.S.A. 112, 8667-8671 (2015). doi:10.1016/j.biosystems.2013.10.003; pmid: 24157699.
80. P. Mähl et al., Twenty year experience of the oral rabies vaccine SAG2 in wildlife: A global review. Vet. Res. 45, 77 (2014). doi:10.1186/s13567-014-0077-8; pmid: 25106552.
81. N. D. Wolfe et al., Emergence of unique primate T-lymphotropic viruses among central African bushmeat hunters. Proc. Natl. Acad. Sci. U.S.A. 102, 7994-7999 (2005). doi:10.1073/pnas.0501734102; pmid: 15911757.
82. J. S. Brashares et al., Bushmeat hunting, wildlife declines, and fish supply in West Africa. Science 306, 1180-1183 (2004). doi:10.1126/science.1102425; pmid: 15539602.
83. P. Daszak, R. Plowright, J. Epstein, J. Pulliam, S. Abdul Rahman, H. Field, C. Smith, K. Olival, S. Luby, K. Halpin, A. D. Hyatt, A. A. Cunningham, in Disease Ecology: Community Structure and Pathogen Dynamics, S. K. Collinge, C. Ray, Eds. (Oxford Univ. Press, Oxford, 2006), pp. 186-201.
84. A. R. Renwick, P. C. L. White, R. G. Bengis, Bovine tuberculosis in southern African wildlife: A multi-species host-pathogen system. Epidemiol. Infect. 135, 529-540 (2007). doi:10.1017/S0950268806007205; pmid: 16959052.
85. A. P. Durbin et al., Emergence potential of sylvatic dengue virus type 4 in the urban transmission cycle is restrained by vaccination and homotypic immunity. Virology 439, 34-41 (2013). doi:10.1016/j.virol.2013.01.018; pmid: 23485373.
86. J. M. Drake et al., Ebola cases and health system demand in Liberia. PLOS Biol. 13, e1002056 (2015). doi:10.1371/journal.pbio.1002056; pmid: 25585384.
87. M. J. Taylor, A. Hoerauf, M. Bockarie, Lymphatic filariasis and onchocerciasis. Lancet 376, 1175-1185 (2010). doi:10.1016/S0140-6736(10)60586-7 pmid: 20739055.
88. E. van Nood et al., Duodenal infusion of donor feces for recurrent Clostridium difficile. N. Engl. J. Med. 368, 407-415 (2013). doi:10.1056/NEJMoa1205037; pmid: 23323867.
89. G. Harms, H. Feldmeier, HIV infection and tropical parasitic diseases - deleterious interactions in both directions? Trop. Med. Int. Health 7, 479-488 (2002). doi:10.1046/j.1365-3156.2002.00893.x; pmid: 12031069.
90. A. A. Hoffmann et al., Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476, 454-457 (2011). doi:10.1038/nature10356; pmid: 21866160.
91. Z. Kambris, P. E. Cook, H. K. Phuc, S. P. Sinkins, Immune activation by life-shortening Wolbachia and reduced filarial competence in mosquitoes. Science 326, 134-136 (2009). doi:10.1126/science.1177531; pmid: 19797660.
92. A. L. Graham, Ecological rules governing helminthmicroparasite coinfection. Proc. Natl. Acad. Sci. U.S.A. 105, 566-570 (2008). doi:10.1073/pnas.0707221105; pmid: 18182496.
93. T. Lembo et al., Exploring reservoir dynamics: A case study of rabies in the Serengeti ecosystem. J. Appl. Ecol. 45, 1246-1257 (2008). doi:10.1111/j.1365-2664.2008.01468.x; pmid: 22427710.
94. K. Hampson et al., Transmission dynamics and prospects for the elimination of canine rabies. PLOS Biol. 7, e53 (2009). pmid: 19278295.
95. A. Pandey et al., Strategies for containing Ebola in West Africa. Science 346, 991-995 (2014). doi:10.1126/science.1260612 pmid: 25414312.
96. E. J. Scholte, F. Schaffner, in Emerging Pests and Vector- Borne Diseases in Europe, W. Takken, B. G. J. Knols, Eds. (Wageningen Academic, Wageningen, Netherlands, 2007), pp. 241-260.
97. S. S. Morse et al., Prediction and prevention of the next pandemic zoonosis. Lancet 380, 1956-1965 (2012). doi:10.1016/S0140-6736(12)61684-5; pmid: 23200504.
98. "PREDICT success: Yellow fever discovered in Bolivian howler monkeys" (One Health Institute, 2014); www.vetmed.ucdavis.edu/ohi/predict/news/bolivia-success-howler-monkeys.cfm.
99. A. D. Blackwell, M. Martin, H. Kaplan, M. Gurven, Antagonism between two intestinal parasites in humans: The importance of co-infection for infection risk and recovery dynamics. Proc. R. Soc. B 280, 20131671 (2013). doi:10.1098/rspb.2013.1671; pmid: 23986108.
100. K. Stiasny et al., Characterization of a structural intermediate of flavivirus membrane fusion. PLOS Pathog. 3, e20 (2007). doi: 10.1371/journal.ppat.0030020.
101. R. M. Anderson, R. M. May, Population biology of infectious diseases: Part I. Nature 280, 361-367 (1979). doi:10.1038/280361a0; pmid: 460412.
102. A. Dobson, Population dynamics of pathogens with multiple host species. Am. Nat. 164 (suppl. 5), S64-S78 (2004). doi:10.1086/424681; pmid: 15540143.
103. L. Gilbert, R. Norman, K. M. Laurenson, H. W. Reid, P. J. Hudson, Disease persistence and apparent competition in a three-host community: An empirical and analytical study of large-scale, wild populations. J. Anim. Ecol. 70, 1053-1061 (2001). doi: 10.1046/j.0021-8790.2001.00558.x.
104. R. Norman, R. G. Bowers, M. Begon, P. J. Hudson, Persistence of tick-borne virus in the presence of multiple host species: Tick reservoirs and parasite mediated competition. J. Theor. Biol. 200, 111-118 (1999). doi:10.1006/jtbi.1999.0982; pmid: 10479543.
105. C. L. Wood, K. D. Lafferty, Biodiversity and disease: A synthesis of ecological perspectives on Lyme disease transmission. Trends Ecol. Evol. 28, 239-247 (2013). doi:10.1016/j.tree.2012.10.011; pmid: 23182683.